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Home , Ballistospore, Hymenium, Spore, Sporocarp (fungi), Stipe (mycology)

fungal ecology 17 (2015) 213e216

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Commentary The shape of fungal ecology: does morphology give clues to a species’ niche?

Pick up any textbook, and you can read about the the spore of a saprotrophic Amanita look somehow con- morphologies of flowers: “most bird flowers are colorful, with sistently different from the spore of a mycorrhizal Amanita? red and yellow ones being the most common. bat flowers are While many modern fungal ecologists may eschew the typically dully colored, and many of them open only at night” study of and sporocarps as throwbacks to a pre- (Raven et al., 1992 pp. 424e425). The color, smell, and shape of molecular era, Peay (2014), Halbwachs et al. (2015) and a flower (as well as quality of and phenology) are used Bassler€ et al. (2014) ask whether there are predictable differ- to predict the kind of associated with a species. For ences between the spores and sporocarps of saprotrophic and example, red flowers that do not smell but produce high ectomycorrhizal fungi. Among other results, Bassler€ et al. quality nectar are associated with hummingbirds, which is (2014) found that saprotrophic fungi produce smaller spor- why hummingbird feeders are often brightly colored and filled ocarps than ectomycorrhizal species, and Halbwachs et al. with strong water. Morphology can be manipulated to (2015) found that spores of ectomycorrhizal species are more attract specific , and syndromes are likely to be ornamented. There are a number of challenges to commonly discussed in the literature (Rosas-Guerrero et al., these kinds of analyses e including, trophic status and spore 2014). are also a clue to ecology, for example, morphology are influenced by phylogeny, and estimating making copious numbers of very small, light, seeds, are likely independent changes in either character requires phyloge- to use wind as a ; seeds with elaiosomes are netically explicit statistical models. Meerts (1999) used phy- likely to be dispersed by ants (Raven et al., 1992). logenetically independent contrasts to demonstrate lineage What about a spore that is ornamented? Can a mycologist specific differences in correlations of spore and know anything about ecology from looking at the shape (Roper sizes. In some cases correlations were positive (for example, et al., 2008) or size of a spore, or the size or phenology of a in and Coprinus) while in other cases, correlations sporocarp? Obviously, morphology is a clue to ; were negative (). While Halbwachs et al. (2015) and look different from . A spore of a Bassler€ et al. (2014) attempt to control for phylogenetic inter- Cordyceps looks like nothing else. dependence, there are reasons to query their assumptions and But perhaps morphology can offer more. The effective methods. For example, the species included in analyses do not dispersal of spores plays an essential role in the ability of fungi form a monophyletic group, although they are treated as a to reach and colonize new substrata. Many spore features are single group, and ancestral state analyses of nutritional mode likely to be under adaptive selective pressures related to the and spore surface characters are not provided. In addition, the particular ecological niche of a species. In fact, the morpho- species are taken from a single geographic region (Northern logical diversity of spores and the sporocarps holding them is Europe), and may be dominated by particular subsets of fungal astonishing (Pringle, 2013), and begs for explanation. In some diversity, including ectomycorrhizal Cortinarius species with cases, morphological diversity is easily explained, for exam- ornamented spores. Nonetheless, both articles ask questions ple, the characteristic forms of hypogeous truffles are the worth thinking about, and provide a valuable path forward. result of natural selection for animal dispersal, and so hypo- If these findings hold, what can they teach us about the geous basidiomycete truffles lack functional sterigmata. selective pressures experienced by fungi in different niches? Understanding these morphologies provides clues in less What is the relationship between spore morphology (specifi- obvious cases, as when a newly discovered epigeous species cally, ornamentation), dispersal, and symbiosis, and why does also lacks sterigmata capable of ballistospore discharge; ani- sporocarp size give a clue to nutritional mode? The ectomy- mal dispersal becomes an obvious hypothesis (Desjardin et al., corrhizal symbiosis has evolved at least 66 times (Tedersoo 2011). But for the majority of spore and sporocarp morpholo- et al., 2010; Tedersoo and Smith, 2013), likely from decom- gies, adaptive significance is unknown. Moreover, we do not poser ancestors in each case. Understanding these transitions know how spore features may or may not relate to a plethora is a major focus of (Hibbett et al., 2000; Bruns and of other ecological strategies e including, for example, does Shefferson, 2004; Wolfe et al., 2012; Kohler et al., 2015). To 214 A. Pringle et al.

date research has emphasized the genetics underpinning the have thought about water. We do know that water can move to symbiosis, and the evolved interaction at the spores: one particularly elegant experiment involved Lyco- interface of a and (Plett and Martin, 2011; Martin perdon perlatum, Fuligo septica, and . Spores of all species and Kohler, 2014; Liao et al., 2014). But the emergence of an were moved from water in a up an inclined glass ectomycorrhizal symbiosis may well involve correlated plane to heights of more than 20 cm (Bandoni and Koske, changes in spore or sporocarp morphology, for example, per- 1974); spores moved up the plane in response to a slow haps a transition to ornamented spores (Halbwachs et al., trickle of water (analogous to rain) that reached and perturbed 2015). the airewater interface in the dish. There is also no doubt that However, to our knowledge there is no research on the water moves species differently, for example, when water is origins of ornamentation, nor do we know if a reversal from poured over soil Penicillium spores do not move well while ornamented to smooth spores has happened in evolutionary spores of Zygorhynchus vuillemini (now moelleri) move history. The critical question is whether or not there is a easily (Burges, 1950). But as with insects, we have a limited fundamental difference in the of saprotrophic and understanding of how effective water is as a vector through ectomycorrhizal fungi, so that each group requires a funda- soil, nor do we really understand potential interactions mentally different dispersal syndrome. Halbwachs et al. (2015) between water and ornamentation. suggest that the predominance of ornamented spores Perhaps ornamentation facilitates movement by animals, amongst ectomycorrhizal fungi is related to the fact that their but inhibits dispersal by water, and perhaps ECM of shallow primary resource (plant ) is buried within the soil matrix, soils benefit from large, ornamented spores, while ECM rather than exposed as are most resources of saprotrophic associated with deep roots benefit from possession of small, fungi. Ornamentation, they hypothesize, may facilitate zoo- smooth spores. This kind of mechanism would help explain or chory by soil invertebrates that would carry the spores closer reinforce the strong patterns of vertical zonation seen in to their destination. Lilleskov and Bruns (2005) showed that many soil fungal communities (Dickie et al., 2002; Taylor et al., the knobby spores of the ectomycorrhizal fungus Tomentella 2014). Perhaps in some cases the depth of a species’ is sublilacina were effectively dispersed on the body of mites, so more of an influence on morphology than trophic status. this is a plausible contention. But it is a single example, and In some cases, literature outside of mycology proves use- we do not know the answers to questions including, is T. ful. For example, the dispersal of bacteria through soil has also sublilacina representative of all ectomycorrhizal species, and been an active area of research. Cell size clearly plays a role in do unornamented spores NOT cling to invertebrates? Do these bacterial dispersal by water; smaller bacteria move more mites really carry the spores from the surface to deeper layers easily with water (Gannon et al., 1991) but soil properties, of soil? However, Halbwachs et al.’s ideas can be tested with specifically the size of the spaces or pores within soil, also experiments, for example to see whether smooth spores are influence migration (Huysman and Verstraete, 1993). Hydro- less effectively dispersed through soil by animals, and phobic bacteria move two to three times more slowly than whether animal dispersal does indeed help move ectomy- hydrophilic strains, because hydrophobic strains stick to soil corrhizal spores deeper into the soil or closer to host particles (Huysman and Verstraete, 1993). Perhaps hydrophilic roots. fungal spores will also move more easily than hydrophobic The hypothesis linking ectomycorrhizal spore orna- fungal spores and, because fungal spores are often coated mentation to animal dispersal is just one of many plausible with numerous hydrophobic proteins, termed conjectures, and for example, the authors might as easily (Whiteford and Spanu, 2002), the potential for species to

20 A B 0.06 C

0.05 15 0.04

10 0.03

0.02 Dry weight (g) Dry weight Cap diameter (cm) diameter Cap

5 51015 0.01 Proportion of Proportion at 50cmspores 0 0.00

51015 51015202530 246810

Cap diameter (cm) Cap height (cm) Cap height (cm)

Fig 1 e Allometric relationships between sporocarp characteristics of ectomycorrhizal fungi. Data are measurements made from 69 sporocarps of 15 species collected at Point Reyes National Seashore by KGP during 2008e2009. Each species is represented by a unique symbol. (A) Relationship between cap diameter and total dry weight. Exponential relationship was fit using the NLS2 package in R. (B) Relationship between cap height (measured from the base of the to the surface of the ) and cap diameter, with best fit linear regression shown. (C) Relationship between height of the hymenium and spore dispersal. Spore dispersal was estimated by counting spore deposits on Vaseline coated glass slides placed overnight at different distances away from marked sporocarps. The figure shows the proportion of observed spores falling in the longest distance class (50 cm) and suggests cap height has a positive effect on mean spore dispersal distances. Shape of fungal ecology 215

evolve differences in hydrophobicity is enormous. However, Bruns, T.D., Shefferson, R.P., 2004. Evolutionary studies of at least one study suggests something quite different: hydro- ectomycorrhizal fungi: recent advances and future directions. e phobins are required for efficient water mediated dispersal of Canadian Journal of Botany 82, 1122 1132. Burges, A., 1950. The downward movement of fungal spores in fulvum (Whiteford and Spanu, 2001). sandy soil. Transactions of the British Mycological Society 33, Complex questions and arguments also surround the link 142e147. € between sporocarp size and nutritional mode (Bassler et al., Dickie, I.A., Xu, B., Koide, R.T., 2002. Vertical niche differentiation 2014). Large sporocarps convey obvious ecological advan- of ectomycorrhizal hyphae in soil as shown by T-RFLP tages. Larger caps provide more surface area for spore pro- analysis. New Phytologist 156, 527e535. duction, and taller enable a higher release point Desjardin, D.E., Peay, K.G., Bruns, T.D., 2011. for spores, making it more likely that spores will travel long squarepantsii: a new species of gasteroid from Borneo. Mycologia 103, 1119e1123. distances (Galante et al., 2011, Fig 1). But these advantages Galante, T.E., Horton, T.R., Swaney, D.P., 2011. 95% of come at a cost, as increasing cap size requires non-linear basidiospores fall within one meter of the cap: a field- and increases in total biomass (Fig 1). Perhaps ectomycorrhizal modeling-based study. Mycologia 103, 1175e1183. fungi can afford larger sporocarps because they access a Gannon, J.T., Manilal, V.B., Alexander, M., 1991. Relationship more predictable source of carbon (Bassler€ et al., 2014), between cell surface properties and transport of bacteria thereby generating the correlation between niche and spor- through soil. Applied and Environmental 57, 190e193. ocarp size. Or perhaps saprotrophic fungi require smaller Halbwachs, H., Brandl, R., Bassler,€ C., 2015. Spore wall traits of sporocarps because species often occupy ephemeral patches ectomycorrhizal and saprotrophic may mirror their of habitat, needing to move among habitats annually, and so distinct lifestyles. Fungal Ecology 17, 197e204. even when resources are scarce or the environment is Hibbett, D.S., Gilbert, L.B., Donoghue, M.J., 2000. Evolutionary suboptimal. Smaller sporocarps may enable consistent instability of ectomycorrhizal symbioses in basidiomycetes. reproduction, year after year. Or perhaps there are other Nature 407, 506e508. explanations. How fungi store and mobilize the carbon and Huysman, F., Verstraete, W., 1993. Water-facilitated transport of bacteria in unsaturated soil columns: influence of cell surface nitrogen needed to produce sporocarps remains an open hydrophobicity and soil properties. Soil and Biochemistry question (Taylor and Alexander, 2005), and one novel tool to 25, 83e90. explore the question would involve tracing the carbon and Kauserud, H., Colman, J.E., Ryvarden, L., 2008. Relationship nitrogen sources for saprotrophic fungi that form large between size, shape and life history sporocarps, for example Agaricus, Macrocybe, Leucopaxillus, characteristics: a comparison of . Fungal Ecology 1, e and Macrolepiota. 19 23. While scientists have thought about the shapes of flowers Kauserud, H., Heegaard, E., Halvorsen, R., Boddy, L., Høiland, K., Stenseth, N.C., 2011. ’s spore size and time of and seeds for hundreds of years, relatively less thought has fruiting are strongly related e is moisture important? Biology been directed at sporocarp or spore morphology, except in Letters 7, 273e276. contexts of taxonomy. Notable exceptions include early work Kohler, A., et al., 2015. Convergent losses of decay mechanisms by A. H. R. Buller, E. Parmasto, C.T. Ingold, and H. Clemenc ¸on, and rapid turnover of symbiosis genes in mycorrhizal and more recent research describing relationships between mutualists. Nature Genetics 47, 410e415. ecological strategies, and sporocarp and spore size, among Liao, H.L., Chen, Y., Bruns, T.D., Peay, K.G., Taylor, J.W., Branco, S., Talbot, J.M., Vilgalys, R., 2014. Metatranscriptomic analysis of polypores and autumnal basidiomycetes (Kauserud et al., ectomycorrhizal roots reveal genes associated with Piloderma- 2008, 2011). The papers by Halbwachs et al. (2015) and Pinus symbiosis: improved methodologies for assessing gene € Bassler et al. (2014) highlight our fundamental ignorance expression in situ. Environmental Microbiology 16, 3730e3742. about basic aspects of natural history, ideally, they will inspire Lilleskov, E.A., Bruns, T.D., 2005. Spore dispersal of a resupinate a new wave of critically needed studies. ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97, 762e769. Martin, F., Kohler, A., 2014. The mycorrhizal symbiosis genomics. In: Martin, F. (Ed.), The Ecological Genomics of Fungi. John Wiley & Sons, Hoboken, NJ, pp. 169e189. Acknowledgments Meerts, P., 1999. The evolution of spore size in Agarics: do big mushrooms have big spores? Journal of Evolutionary Biology 12, e An anonymous reviewer provided very helpful comments on 161 165. Peay, K.G., 2014. Back to the future: natural history and the way a draft of this commentary. forward in modern fungal ecology. Fungal Ecology 12, 4e9. Plett, J.M., Martin, F., 2011. Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends in Genetics 27, 14e22. references Pringle, A., 2013. Asthma and the diversity of fungal spores in air. PLOS Pathogens 9 (6), e1003371. Raven, P.H., Evert, R.F., Eichhorn, S.E., 1992. Biology of Plants, fifth Bandoni, R.J., Koske, R.E., 1974. Monolayers and microbial edn. Worth Publishers, New York, NY. dispersal. Science 183, 1079e1081. Roper, M., Pepper, R., Brenner, M.P., Pringle, A., 2008. Explosively Bassler,€ C., Heilmann-Clusen, J., Karasch, P., Brandl, R., launched spores of ascomycete fungi have drag minimizing Halbwachs, H., 2014. Ectomycorrhizal fungi have larger fruit shapes. Proceedings of the National Academy of Sciences 105, e bodies than saprotrophic fungi. Fungal Ecology 17, 205e212. 20583 20588. 216 A. Pringle et al.

Rosas-Guerrero, V., Aguilar, R., Marten-Rodrıguez, S., article info Ashworth, L., Lopezaraiza-Mikel, M., Bastida, J.M., Quesada, M., 2014. A quantitative review of pollination Accepted 15 April 2015 syndromes: do floral traits predict effective pollinators? Ecology Letters 17, 388e400. Corresponding editor: Lynne Boddy Taylor, D.L., Hollingsworth, T.N., McFarland, J.W., Lennon, N.J., Nusbaum, C., Ruess, R.W., 2014. A first comprehensive census keywords of fungi in soil reveals both hyperdiversity and fine-scale Allometry niche partitioning. Ecological Monographs 84, 3e20. Taylor, A.F.S., Alexander, I., 2005. The ectomycorrhizal symbiosis: Fruit body life in the real world. Mycologist 19, 102e112. Mushroom Tedersoo, L., May, T.W., Smith, M.E., 2010. Ectomycorrhizal Mycology lifestyle in fungi: global diversity, distribution, and evolution Size e of phylogenetic lineages. 20, 217 263. Sporocarp Tedersoo, L., Smith, M.E., 2013. Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal Biology Reviews 27, Anne PRINGLEa,*, Else VELLINGAb, Kabir PEAYc 83e99. Whiteford, J.R., Spanu, P.D., 2002. Hydrophobins and the aHarvard Forest, 324 N. Main St., Petersham, MA 01366, USA interactions between fungi and plants. Molecular Plant bDept. of Plant and Microbial Biology, Berkeley, CA 94720, USA Pathology 3, 391e400. cDept. of Biology, Stanford University, Stanford, CA 94305, USA Whiteford, J.R., Spanu, P.D., 2001. The HCf-1 of Cladosporium fulvum is required for efficient water- *Corresponding author. mediated dispersal of conidia. Fungal Genetics and Biology E-mail address: [email protected] (A. Pringle). 32, 159e168. Wolfe, B.E., Tulloss, R.E., Pringle, A., 2012. The irreversible loss of 1754-5048/$ e see front matter a decomposition pathway marks the single origin of an ª 2015 Elsevier Ltd and The British Mycological Society. ectomycorrhizal symbiosis. PLoS One 7 (7), e39597. http://dx.doi.org/10.1016/j.funeco.2015.04.005